Endothelial Jagged1 levels and distribution are post-transcriptionally controlled by ZFP36 decay proteins

Cell Rep. 2024 Jan 23;43(1):113627. doi: 10.1016/j.celrep.2023.113627. Epub 2023 Dec 28.

Abstract

Vascular morphogenesis requires a delicate gradient of Notch signaling controlled, in part, by the distribution of ligands (Dll4 and Jagged1). How Jagged1 (JAG1) expression is compartmentalized in the vascular plexus remains unclear. Here, we show that Jag1 mRNA is a direct target of zinc-finger protein 36 (ZFP36), an RNA-binding protein involved in mRNA decay that we find robustly induced by vascular endothelial growth factor (VEGF). Endothelial cells lacking ZFP36 display high levels of JAG1 and increase angiogenic sprouting in vitro. Furthermore, mice lacking Zfp36 in endothelial cells display mispatterned and increased levels of JAG1 in the developing retinal vascular plexus. Abnormal levels of JAG1 at the sprouting front alters NOTCH1 signaling, increasing the number of tip cells, a phenotype that is rescued by imposing haploinsufficiency of Jag1. Our findings reveal an important feedforward loop whereby VEGF stimulates ZFP36, consequently suppressing Jag1 to enable adequate levels of Notch signaling during sprouting angiogenesis.

Keywords: CP: Cell biology; CP: Molecular biology; RNA-decay; VEGF; angiogenesis; notch; tristetraproline; vascular morphogenesis.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / metabolism
  • Cell Proliferation
  • Endothelial Cells / metabolism
  • Jagged-1 Protein / genetics
  • Jagged-1 Protein / metabolism
  • Membrane Proteins* / genetics
  • Membrane Proteins* / metabolism
  • Mice
  • Neovascularization, Physiologic
  • Receptors, Notch / metabolism
  • Signal Transduction
  • Vascular Endothelial Growth Factor A* / genetics
  • Vascular Endothelial Growth Factor A* / metabolism

Substances

  • Calcium-Binding Proteins
  • Jagged-1 Protein
  • Membrane Proteins
  • Receptors, Notch
  • Vascular Endothelial Growth Factor A
  • Zfp36 protein, mouse
  • Jag1 protein, mouse